Concurrent human TMS-EEG-fMRI enables monitoring of oscillatory brain state-dependent gating of cortico-subcortical network activity

Abstract

Despite growing interest, the causal mechanisms underlying human neural network dynamics remain elusive. Transcranial Magnetic Stimulation (TMS) allows to noninvasively probe neural excitability, while concurrent fMRI can log the induced activity propagation through connected network nodes. However, this approach ignores ongoing oscillatory fluctuations which strongly affect network excitability and concomitant behavior. Here, we show that concurrent TMS-EEG-fMRI enables precise and direct monitoring of causal dependencies between oscillatory states and signal propagation throughout cortico-subcortical networks. To demonstrate the utility of this multimodal triad, we assessed how pre-TMS EEG power fluctuations influenced motor network activations induced by subthreshold TMS to right dorsal premotor cortex. In participants with adequate motor network reactivity, strong pre-TMS alpha power reduced TMS-evoked hemodynamic activations throughout the bilateral cortico-subcortical motor system (including striatum and thalamus), suggesting shunted network connectivity. Concurrent TMS-EEG-fMRI opens an exciting noninvasive avenue of subject-tailored network research into dynamic cognitive circuits and their dysfunction.

Combining transcranial magnetic stimulation with functional magnetic resonance imaging for probing and modulating neural circuits relevant to affective disorders

“…A growing body of evidence outlines a role for neural rhythms in statedependence as well. Pre-stimulation alpha power influences TMS-evoked BOLD response (Peters et al, 2020) and TMS-evoked neuronal oscillatory activity has been correlated with individual differences in cognitive ability (Ozdemir et al, 2020), for example.…”

Reliability of transcranial magnetic stimulation evoked potentials to detect the effects of theta-burst stimulation of the prefrontal cortex

“…Several variables may contribute to between-sessions variability, which is likely to impact the test-retest reliability levels of TBS effects. Past evidence suggests that TEPs are sensitive to variations in brain state (Peters et al, 2020), level of fatigue (Otieno et al, 2019), vigilance state (Massimini et al, 2005) and movement initiation (Nikulin et al, 2003). The level of vigilance with time awake from the morning also seems to impact cortical responsiveness to TMS (Manganotti et al, 2013, Huber et al, 2013).…”

Multi-scale neural decoding and analysis

“…The simultaneous acquisition of neuronal and hemodynamic responses along with stimulation can provide an objective form of feedback to guide the stimulation procedure, quantify the stimulation effects, and investigate the underlying neural dynamics [246,[250][251][252]. Furthermore, the combination of fMRI and EEG with concurrent stimulation can further elucidate the effects of stimulation on connected brain regions [145,253]. However, a major challenge with simultaneous stimulation and measurement is the introduction of strong artifacts in the obtained signal.…”